The Nitric Oxide-guanylyl Cyclase Signaling Pathway Modulates Membrane Activity States and Electrophysiological Properties of Striatal Medium Spiny Neurons Recorded in Vivo

Overview

Journal J Neurosci

Specialty Neurology

Date 2004 Feb 27

PMID 14985433

Citations 43

Authors

Anthony R West

Anthony A Grace

Affiliations

Soon will be listed here.

Abstract

Nitric oxide (NO)-releasing interneurons are believed to regulate the activity of striatal medium spiny neurons (MSNs) that contain the NO effector enzyme guanylyl cyclase (GC). The involvement of NO-GC signaling in modulating steady-state membrane activity of striatal MSNs was examined using in vivo intracellular recordings in rats. Intrastriatal infusion of a neuronal NO synthase inhibitor or a NO scavenger via reverse microdialysis consistently decreased the amplitude of spontaneously occurring depolarized plateau potentials (up events). Intrastriatal infusion of a NO scavenger also decreased the amplitude of EPSPs evoked during electrical stimulation of the orbital prefrontal cortex. The effect of the NO scavenger on spontaneous up events was partially reversed by coperfusion with a cell-permeable cGMP analog. Intracellular injection of MSNs with a soluble GC inhibitor resulted in large decreases in the following: (1) spontaneous up-event amplitude, (2) responsiveness to depolarizing current, (3) action potential amplitude, and (4) input resistance. These effects were partially reversed by coinjection of cGMP. Conversely, intracellular injection of a phosphodiesterase inhibitor increased MSN neuron membrane excitability. These results indicate that, in the intact animal, the NO signaling pathway exerts a powerful tonic modulatory influence over the membrane activity of striatal MSNs via the activation of GC and stimulation of cGMP production.

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References

Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M . A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci. 1999; 19(7):2489-99. PMC: 6786075. View

Calabresi P, Centonze D, Gubellini P, Marfia G, Bernardi G . Glutamate-triggered events inducing corticostriatal long-term depression. J Neurosci. 1999; 19(14):6102-10. PMC: 6783059. View

Greengard P, Allen P, Nairn A . Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron. 1999; 23(3):435-47. DOI: 10.1016/s0896-6273(00)80798-9. View

Hokfelt T, Ubink R, Lubec G, Herrera-Marschitz M . Neurocircuitries of the basal ganglia studied in organotypic cultures: focus on tyrosine hydroxylase, nitric oxide synthase and neuropeptide immunocytochemistry. Neuroscience. 2000; 94(4):1133-51. DOI: 10.1016/s0306-4522(99)00415-7. View

de Vente J, Markerink-van Ittersum M, van Abeelen J, Emson P, Axer H, Steinbusch H . NO-mediated cGMP synthesis in cholinergic neurons in the rat forebrain: effects of lesioning dopaminergic or serotonergic pathways on nNOS and cGMP synthesis. Eur J Neurosci. 2000; 12(2):507-19. DOI: 10.1046/j.1460-9568.2000.00927.x. View

Calabresi P, Centonze D, Gubellini P, Marfia G, Pisani A, Sancesario G . Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol. 2000; 61(3):231-65. DOI: 10.1016/s0301-0082(99)00030-1. View

West A, Grace A . Striatal nitric oxide signaling regulates the neuronal activity of midbrain dopamine neurons in vivo. J Neurophysiol. 2000; 83(4):1796-808. DOI: 10.1152/jn.2000.83.4.1796. View

Sahach V, Baziliuk O, Oleshko M, Kotsiuruba O, Bukhanevych O, Appenzeller O . [The nitric oxide system in a chronic deficiency of mesostriatal dopamine: the action of nitroglycerin]. Fiziol Zh (1994). 2000; 46(2):55-63. View

Sancesario G, Morello M, Reiner A, Giacomini P, Massa R, Schoen S . Nitrergic neurons make synapses on dual-input dendritic spines of neurons in the cerebral cortex and the striatum of the rat: implication for a postsynaptic action of nitric oxide. Neuroscience. 2000; 99(4):627-42. DOI: 10.1016/s0306-4522(00)00227-x. View

10.

Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K . Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci. 2000; 20(22):8443-51. PMC: 6773171. View

11.

Hidaka S, Totterdell S . Ultrastructural features of the nitric oxide synthase-containing interneurons in the nucleus accumbens and their relationship with tyrosine hydroxylase-containing terminals. J Comp Neurol. 2001; 431(2):139-54. DOI: 10.1002/1096-9861(20010305)431:2<139::aid-cne1061>3.0.co;2-0. View

12.

West A, Grace A . Opposite influences of endogenous dopamine D1 and D2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci. 2002; 22(1):294-304. PMC: 6757590. View

13.

Cavas M, Navarro J . Coadministration of L-NOARG and tiapride: effects on catalepsy in male mice. Prog Neuropsychopharmacol Biol Psychiatry. 2002; 26(1):69-73. DOI: 10.1016/s0278-5846(01)00231-7. View

14.

Sanchez J, Abreu P, Gonzalez M . Sodium nitroprusside stimulates L-DOPA release from striatal tissue through nitric oxide and cGMP. Eur J Pharmacol. 2002; 438(1-2):79-83. DOI: 10.1016/s0014-2999(02)01286-4. View

15.

West A, Galloway M, Grace A . Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse. 2002; 44(4):227-45. DOI: 10.1002/syn.10076. View

16.

West A, Moore H, Grace A . Direct examination of local regulation of membrane activity in striatal and prefrontal cortical neurons in vivo using simultaneous intracellular recording and microdialysis. J Pharmacol Exp Ther. 2002; 301(3):867-77. DOI: 10.1124/jpet.301.3.867. View

17.

Reed T, Repaske D, Snyder G, Greengard P, Vorhees C . Phosphodiesterase 1B knock-out mice exhibit exaggerated locomotor hyperactivity and DARPP-32 phosphorylation in response to dopamine agonists and display impaired spatial learning. J Neurosci. 2002; 22(12):5188-97. PMC: 6757711. View

18.

Marin P, Lafon-Cazal M, Bockaert J . A Nitric Oxide Synthase Activity Selectively Stimulated by NMDA Receptors Depends on Protein Kinase C Activation in Mouse Striatal Neurons. Eur J Neurosci. 1992; 4(5):425-432. DOI: 10.1111/j.1460-9568.1992.tb00892.x. View

19.

Di Giovanni G, Ferraro G, Sardo P, Galati S, Esposito E, La Grutta V . Nitric oxide modulates striatal neuronal activity via soluble guanylyl cyclase: an in vivo microiontophoretic study in rats. Synapse. 2003; 48(2):100-7. DOI: 10.1002/syn.10193. View

20.

Ariano M . Distribution of components of the guanosine 3',5'-phosphate system in rat caudate-putamen. Neuroscience. 1983; 10(3):707-23. DOI: 10.1016/0306-4522(83)90212-9. View